Skip to main content
SpringerLink
Log in

Hybridization between insular endemic and widespread species of Viola in non-disturbed environments assessed by nuclear ribosomal and cpDNA sequences

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Viola jaubertiana Marès & Vigin. is a narrow endemic violet of the Balearic Islands, restricted to small, fragmented, and scattered populations living in inaccessible rocky places and calcareous overhangs. V. jaubertiana is entirely glabrous and morphologically very uniform. However, several authors have reported hairy individuals collected at the type locality, suggesting that these rupicolous, pubescent plants are putative hybrids with V. alba Bess. subsp. dehnhardtii (Ten.) W. Becker, a woodland violet growing in the area. Ribosomal ITS sequences of the putative hybrids analysed showed additive species-specific sites of V. alba subsp. dehnhardtii and V. jaubertiana, strongly supporting its hybrid origin from these progenitors. CpDNA sequences of all putative hybrids were uniform, and identical to those present in V. jaubertiana accessions. This suggests that the gene flow between V. alba subsp. dehnhardtii and V. jaubertiana is unidirectional and identifies the endemic V. jaubertiana as the unique ovule donor. The additivity of the ITS sequences, together with the pollen and ovule sterility, suggests that the sampled individuals are primary F1 hybrids, whereas no trace of introgressive hybridization or hybrid zone has been evidenced by the nuclear and plastid markers used. Judging from herbarium sheets, hybridization between V. alba subsp. dehnhardtii and V. jaubertiana is recurrent and dates back from the XIXth century. Hybrids between these species are not linked to disturbed environments. In fact, they have been always reported in rupicolous habitats, where the maternal species is restricted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abbot R (1992) Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol 7:401–405

    Article  Google Scholar 

  • Álvarez I., Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Molec Phylogenet Evol 29:417–434

    Article  PubMed  Google Scholar 

  • Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn R (eds) Evolution of genes and proteins. Sinauer, Sunderland, pp 38–61

    Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Arnold ML (2006) Evolution through genetic exchange. Oxford University Press, Oxford

    Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman & Hall, New York

    Google Scholar 

  • Ballard HE Jr, Sytsma KJ, Kowal RR (1999) Shrinking the violets: phylogenetic relationships of infrageneric groups in Viola (Violaceae) based on internal transcribed spacer DNA sequences. Syst Bot 23:439–458

    Article  Google Scholar 

  • Beattie AJ, Lyons N (1975) Seed dispersal in Viola (Violaceae): adaptations and strategies. Amer J Bot 62:714–722

    Article  Google Scholar 

  • Brochmann C (1984) Hybridization and distribution of Argyranthemum coronopifolium (Asteraceae-Anthemidae) in the Canary Islands. Nord J Bot 4:729–736

    Article  Google Scholar 

  • Buckler ESI, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA: divergent paralogous and phylogenetic implications. Genetics 145:821–832

    PubMed  CAS  Google Scholar 

  • Buerkle CA, Wolf DE, Rieseberg LH (2003) The origin and extinction of species through hybridization. In: Brigham CA, Schwartz MW (eds) Population viability in plants. Springer, Berlin, pp 117–141

    Google Scholar 

  • Burnat E, Barbey W (1882) Notes sur un voyage botanique dans les îles Baléares et dans la province de Valence (Espagne). Mai–Juin, 1881. H. George, Genève and Bâle

  • Chodat L (1924) Contributions à la Géo-Botanique de Majorque. Bull Soc Bot Genève ser.2, 15:153–264

    Google Scholar 

  • Contandriopoulos J, Cardona MA (1984) Caractère original de la flore endémique des Baléares. Bot Helvet 94:101–131

    Google Scholar 

  • Crockett SL, Douglas AW, Scheffler BE, Khan IA (2004) Genetic profiling of Hypericum L. (St. John’s Wort) species by nuclear ribosomal ITS sequence analysis. Planta Med 70:929–935

    Article  PubMed  CAS  Google Scholar 

  • Culley TM (2002) Reproductive biology and selfing rates in Viola pubescens (Violaceae), and understory herb with chasmogamous and cleistogamous flowers. Int J Pl Sci 163:113–122

    Article  Google Scholar 

  • Davis PH (1951) Cliff vegetation in the Eastern Mediterranean. J Ecol 39:63–93

    Article  Google Scholar 

  • Dover G (1994) Concerted evolution, molecular drive and natural selection. Curr Biol 4:1165–1166

    Article  PubMed  CAS  Google Scholar 

  • Doyle J, Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Erben M (1996) The significance of hybridization on the forming species in the genus Viola. Bocconea 5:113–118

    Google Scholar 

  • Fuertes-Aguilar J, Rosselló JA, Nieto-Feliner G (1999) Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae). Molec Ecol 8:1341–1346

    Article  CAS  Google Scholar 

  • Galbany-Casals M, García-Jacas N, Susana A, Sáez L, Benedí C (2004) Phylogenetic relationships in the Mediterranean Helichrysum (Asteraceae, Gnaphalieae) based on nuclear rDNA ITS sequence data. Austral Syst Bot 17:241–253

    Article  CAS  Google Scholar 

  • Grant V (1981) Plant speciation. Columbia University Press, New York

    Google Scholar 

  • Harris SA, Ingram R (1991) Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon 40:393–412

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Molec Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Krahulcova A, Krahulec F, Kirschner J (1996) Introgressive hybridization between a native and an introduced species: Viola lutea subsp. sudetica versus V. tricolor. Folia Geobot 31:219–244

    Article  Google Scholar 

  • Lai Z, Gross B, Zou Y, Andrews J, Rieseberg LH (2006) Detecting differential gene expression in homoploid hybrid sunflower species using microarrays. Molec Ecol 15:1213–1227

    Article  CAS  Google Scholar 

  • Levin DA (2000) The origin, expansion, and demise of plant species. Oxford University Press, Oxford

    Google Scholar 

  • Levin DA, Francisco-Ortega JF, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 15:10–16

    Article  Google Scholar 

  • Malécot V, Marcussen T, Munzinger J, Yockteng R, Henry M (2007) On the origin of the sweet-smelling Parma violet cultivars (Violaceae): wide intraspecific hybridization, sterility, and sexual reproduction. Amer J Bot 94:29–41

    Article  Google Scholar 

  • Marcussen T, Borgen L (2000) Allozymic variation and relationships within Viola subsection Viola (Violaceae). Pl Syst Evol 223:29–57

    Article  CAS  Google Scholar 

  • Marcussen T, Nordal I (1998) Viola suavis, a new species in the Nordic flora, with analyses of the relation to other species in subsection Viola (Violaceae). Nordic J Bot 18:221–237

    Article  Google Scholar 

  • Marcussen T, Borgen L, Nordal I (2001) Viola hirta and its relatives in Norway. Nordic J Bot 21:5–17

    Article  Google Scholar 

  • Marès P, Vigineix G (1880) Catalogue raisonné des plantes vasculaires des Iles Baléares. G. Masson, Paris

  • Mus M, Sáez L, Rosselló JA (2000) Viola barceloi Nyman, V. barceloi L. Chodat and V. suavis var. barceloi O. Bolos & Vigo: too many eponyms or too many taxa? Taxon 49:785–788

    Article  Google Scholar 

  • Nasrallah ME, Yogeeswaran K, Snyder S, Nasrallah JB (2000) Arabidopsis species hybrids in the study of species differences and evolution of amphiploidy in plants. Pl Physiol 124:1605–1614

    Article  CAS  Google Scholar 

  • Neuffer B, Auge H, Mesch H, Amarell U, Brandl R (1999) Spread of violets in polluted pine forests: morphological and molecular evidence for the ecological importance of interspecific hybridization. Molec Ecol 8:365–377

    Google Scholar 

  • Nieto-Feliner G, Gutiérrez-Larena B, Fuertes-Aguilar J (2004) Fine scale geographical structure, intra-individual polymorphism and recombination in nuclear ribosomal internal transcribed spacers in Armeria (Plumbaginaceae). Ann Bot 93:189–200

    Article  PubMed  Google Scholar 

  • Oh BJ, Ko MK, Lee CH (1998) Identification of the series-specific random amplified polymorphic DNA markers of Viola species. Pl Breed 117:295–296

    Article  Google Scholar 

  • Rieseberg LH (1995) The role of hybridization in evolution: old wine in new skins. Amer J Bot 82:944–953

    Article  Google Scholar 

  • Ritland CE, Ritland RK, Straus NA (1993) Variation in the ribosomal internal transcribed spacers (ITS1 and ITS2) among eight taxa of the Mimulus guttatus species complex. Molec Biol Evol 10:1273–1288

    PubMed  CAS  Google Scholar 

  • Rosselló JA, Sáez L (2001) Index balearicum: an annotated check-list of the vascular plants described from the Balearic Islands. Collect Bot (Barcelona) 25:1–192

    Google Scholar 

  • Rosselló JA, Mayol M, Mus M, Torres N (1991) Taxonomia i nomenclatura de plantes baleàriques. Boll Soc Hist Nat Balears 32:153–154

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annual Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molec Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schmidt A (1961) Zytotaxonomische Untersuchungen an europäischen Viola-Arten der Sektion Nomimium. Oester Bot Zeitschr 108:20–88

    Article  Google Scholar 

  • Simmons RE, Griffin M, Griffin RE, Marais E, Kolberg H (1998) Endemism in Namibia: patterns, processes and predictions. Biodiv Conserv 7:513–530

    Article  Google Scholar 

  • Siuta A, Bozek M, Jedrzejczyk M, Rostanski A, Kuta E (2005) Is the blue zinc violet (Viola guestphalica Nauenb.) a taxon of hybrid origin? Evidence from embryology. Acta Biol Crac Ser Bot 47:237–245

    Google Scholar 

  • Soltis PS, Soltis DE (1991) Multiple origins of the allotetraploid Tragopogon mirus (Compositae): rDNA evidence. Syst Bot 16:407–413

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), 4th edn, Sinauer, Sunderland

  • Sytsma KJ, Smith JF (1992) Molecular systematics of Onagraceae: examples from Clarkia and Fuchsia. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman & Hall, New York, pp 295–323

    Google Scholar 

  • Taberlet P, Gielly L, Patou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109

    Article  CAS  Google Scholar 

  • Tchourina O (1909) Note sur le Viola jaubertiana Marès. Bull Soc Bot Genève Ser. 2, 1:204–207

    Google Scholar 

  • Ungerer MC, Baird SJE, Pan J, Rieseberg LH (1998) Rapid hybrid speciation in wild sunflowers. Proc Natl Acad Sci USA 95:11757–11762

    Article  Google Scholar 

  • Valentine DH (1949) The experimental taxonomy of two species of Viola. New Phytol 49:194–212

    Google Scholar 

  • Valentine DH (1958) Cytotaxonomy of the rostrate violets. Proc Linn Soc Lond 169:132–134

    Google Scholar 

  • Valentine DH (1975) Viola L. In: Stace CA (ed) Hybridization and the Flora of the British Isles. Academic Press, London, pp 154–163

    Google Scholar 

  • Wendel JF, Schnabel A, Seelanan T (1995) Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92:280–284

    Article  PubMed  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Yockteng R, Ballard HE, Mansion G, Dajoz I, Nadot S (2003) Relationships among pansies (Viola section Melanium) investigated using ITS and ISSR markers. Pl Syst Evol 241:153–170

    Article  Google Scholar 

  • Yoo K-O, Jang S-K, Lee W-T (2005) Phylogeny of Korean Viola based on ITS sequences. Korean J Pl Taxonomy 35:7–23

    Google Scholar 

Download references

Acknowledgments

We are indebted to our colleague Arántzazu Molins for her generous help throughout the field sampling and lab work. Relevant samples were provided by Pere Fraga and the staff of the Botanical Garden of Sóller (Balearic Islands). We thank Gonzalo Nieto-Feliner for friendly discussions, and the comments of two anonymous reviewers that improved the manuscript. This work has been partially funded by the CGL2007-60550/BOS project.

Author information

Authors and Affiliations

  1. Botànica, Departament de Biologia, Universitat de les Illes Balears, 07122, Balearic Islands, Palma de Mallorca, Spain

    M. À. Conesa & M. Mus

  2. Jardín Botánico, Universidad de Valencia, c/Quart 80, 46008, Valencia, Spain

    J. A. Rosselló

Authors
  1. M. À. Conesa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Mus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. A. Rosselló
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. A. Rosselló.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Conesa, M.À., Mus, M. & Rosselló, J.A. Hybridization between insular endemic and widespread species of Viola in non-disturbed environments assessed by nuclear ribosomal and cpDNA sequences. Plant Syst Evol 273, 169–177 (2008). https://doi.org/10.1007/s00606-008-0006-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-008-0006-2

Keywords

Search

Navigation